Gastric and pyloric motor pattern control by a modulatory projection neuron in the intact crab Cancer pagurus

Journal of Neurophysiology

Volumn 105, Issue 4, 2011, Pages 1671-1680

  Hedrich, Ulrike B S ^a   Diehl, Florian ^b   Stein, Wolfgang ^b  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY OF ULM   (Germany)

Author keywords

Central pattern generator; Descending control; Neuromodulation; Sensorimo tor; Stomatogastric nervous system

Indexed keywords

ANIMAL EXPERIMENT; ANTENNA (ORGAN); ARTICLE; CANCER PAGURUS; CONTROLLED STUDY; CORRELATIONAL STUDY; CRAB; IN VITRO STUDY; IN VIVO STUDY; MODULATION; MODULATORY PROJECTION NEURON 1; MOTOR ACTIVITY; NERVE CELL; NERVE FIBER; NERVE PROJECTION; NONHUMAN; PRIORITY JOURNAL; PYLORUS; RHYTHM; SENSORIMOTOR FUNCTION; SENSORY STIMULATION; STIMULATION; STOMACH MOTILITY;

ANIMALS; BRACHYURA; GANGLIA, INVERTEBRATE; MOTOR NEURONS; NEURAL PATHWAYS; PYLORUS; STOMACH;

EID: 79955145789     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.01105.2010     Document Type: Article

References (60)

1. Antri M, Fenelon K, Dubuc R. The contribution of synaptic inputs to sustained depolarizations in reticulospinal neurons. J Neurosci 29: 1140- 1151,2009.
2. Audsley N, Weaver RJ. Neuropeptides associated with the regulation of feeding in insects. Gen Comp Endocrinol 162: 93-104, 2009.
3. Bartos M, Nusbaum MP. Intercircuit control of motor pattern modulation by presynaptic inhibition. J Neurosci 17: 224-2256, 1997.
4. Beenhakker MP, Blitz DM, Nusbaum MP. Long-lasting activation of rhyth- mic neuronal activity by a novel mechanosensory system in the crustacean stomatogastric nervous system. J Neurophysiol 91: 78-91, 2004.
5. Beenhakker MP, DeLong ND, Saideman SR, Nadim F, Nusbaum MP. Proprioceptor regulation of motor circuit activity by presynaptic inhibition of a modulatory projection neuron. J Neurosci 25: 8794-8806, 2005.
6. Birmingham JT, Tauck DL. Neuromodulation in invertebrate sensory sys- tems: from biophysics to behavior. J Exp Biol 206: 3541-3546, 2003.
7. Blitz DM, Nusbaum MP. Motor pattern selection via inhibition of parallel pathways. J Neurosci 17: 4965-4975, 1997.
8. Blitz DM, Nusbaum MP. State-dependent presynaptic inhibition regulates central pattern generator feedback to descending inputs. J Neurosci 28: 9564-9574, 2008.
9. Blitz DM, Beenhakker MP, Nusbaum MP. Different sensory systems share projection neurons but elicit distinct motor patterns. J Neurosci 24: 11381- 11390,2004.
10. Blitz DM, White RS, Saideman SR, Cook A, Christie AE, Nadim F, Nusbaum MP. A newly identified extrinsic input triggers a distinct gastric mill rhythm via activation of modulatory projection neurons. J Exp Biol 211: 1000-1011, 2008.
11. Böhm H, Dybek E, Heinzel HG. Anatomy, and in vivo activity of neurons connecting the crustacean stomatogastric nervous system to the brain. J Comp Physiol A 187: 393-403, 2001.
12. Brezina V. Beyond the wiring diagram: signalling through complex neuro- modulator networks. Philos Trans R Soc Lond B Biol Sci 365: 2363-2374, 2010.
13. Brock F. Das Verhalten der ersten Antennen von Brachyuren und Anomuren in Bezug auf das umgebende Medium. J Comp Physiol A 11: 774-790, 1930.
14. Calabrese RL. Behavioral choices: how neuronal networks make decisions. Curr Biol 13: R140-142, 2003.
15. Cantrell AR, Catterall WA. Neuromodulation of Na channels: an unex- pected form of cellular plasticity. Nat Rev Neurosci 2: 397-407, 2001.
16. Chen R, Ma M, Hui L, Zhang J, Li L. Measurement of neuropeptides in crustacean hemolymph via MALDI mass spectrometry. J Am Soc Mass Spectrom 20: 708-718, 2009.
17. Christie AE, Stein W, Quinlan JE, Beenhakker MP, Marder E, Nusbaum MP. Actions of a histaminergic/peptidergic projection neuron on rhythmic motor patterns in the stomatogastric nervous system of the crab Cancer borealis. J Comp Neurol 469: 153-169, 2004.
18. Coleman MJ, Meyrand P, Nusbaum MP. A switch between two modes of synaptic transmission mediated by presynaptic inhibition. Nature 378: 502-505, 1995.
19. Dickinson PS. Neuromodulation of central pattern generators in invertebrates and vertebrates. Curr Opin Neurobiol 16: 604-614, 2006.
20. Eaton RC, Lee RK, Foreman MB. The Mauthner cell and other identified neurons of the brainstem escape network of fish. Prog Neurobiol 63: 467-485, 2001.
21. Esch T, Kristan WB Jr. Decision-making in the leech nervous system. Integr Comp Biol 42: 716, 2002.
22. Esch T, Mesce KA, Kristan WB. Evidence for sequential decision making in the medicinal leech. J Neurosci 22: 11045-11054, 2002.
23. Grillner S, Cangiano L, Hu GY, Thompson R, Hill R, Wallén P. The intrinsic function of a motor system-from ion channels to networks and behavior. Brain Res 886: 224-236, 2000.
24. Gu Q. Neuromodulatory transmitter systems in the cortex and their role in cortical plasticity. Neuroscience 111: 815-835, 2002.
25. Gutierrez GJ, Grashow RG. Cancer borealis stomatogastric nervous system dissection. J Vis Exp 25: 1207, 2009.
26. Harris-Warrick RM, Johnson BR. Checks and balances in neuromodulation. Front Behav Neurosci 4: 47, 2010.
27. Hedrich UB, Stein W. Characterization of a descending pathway: activation and effects on motor patterns in the brachyuran crustacean stomatogastric nervous system. J Exp Biol 211: 2624-2637, 2008.
28. Hedrich UB, Smarandache CR, Stein W. Differential activation of projec- tion neurons by two sensory pathways contributes to motor pattern selection. J Neurophysiol 102: 2866-2879, 2009.
29. Heinzel HG, Weimann JM, Marder E. The behavioral repertoire of the gastric mill in the crab, Cancer pagurus: an in situ endoscopic, and electrophysiological examination. J Neurosci 13: 1793-1803, 1993.
30. Jing J, Vilim FS, Cropper EC, Weiss KR. Neural analog of arousal: persistent conditional activation of a feeding modulator by serotonergic initiators of locomotion. J Neurosci 28: 12349-12361, 2008.
31. Katz PS. Comparison of extrinsic and intrinsic neuromodulation in two central pattern generator circuits in invertebrates. Exp Physiol 83: 281-292, 1998.
32. Katz PS. Beyond Neurotransmission: Neuromodulation and Its Importance for Information Processing. New York: Oxford University Press, 1999.
33. Katz PS, Frost WN. Intrinsic neuromodulation: altering neuronal circuits from within. Trends Neurosci 19: 54-61, 1996.
34. Katz PS, Eigg MH, Harris-Warrick RM. Serotonergic/cholinergic muscle receptor cells in the crab stomatogastric nervous system. I. Identification and characterization of the gastropyloric receptor cells. J Neurophysiol 62: 558-570, 1989.
35. Krichmar JL. The neuromodulatory system: a framework for survival and adaptive behavior in a challenging world. Adapt Behav 16: 385-399, 2008.
36. Luther JA, Robie AA, Yarotsky J, Reina C, Marder E, Golowasch J. Episodic bouts of activity accompany recovery of rhythmic output by a neuromodulator- and activity-deprived adult neural network. J Neurophysiol 90: 2720-2730, 2003.
37. Marder E, Calabrese RL. Principles of rhythmic motor pattern generation. Physiol Rev 76: 687-717, 1996.
38. Marder E, Bucher D. Understanding circuit dynamics using the stomatogas- tric nervous system of lobsters and crabs. Annu Rev Physiol 69: 291-316, 2007.
39. Marder E, Bucher D, Schulz DJ, Taylor AL. Invertebrate central pattern generation moves along. Curr Biol 15: R685-699, 2005.
40. Morgan PT, Jing J, Vilim FS, Weiss KR. Interneuronal and peptidergic control of motor pattern switching in Aplysia. J Neurophysiol 87: 49-61, 2002.
41. Neumeister H, Szabo TM, Preuss T. Behavioral and physiological charac- terization of sensorimotor gating in the goldfish startle response. J Neuro- physiol 99: 1493-1502, 2008.
42. Norris BJ, Coleman MJ, Nusbaum MP. Pyloric motor pattern modification by a newly identified projection neuron in the crab stomatogastric nervous system. J Neurophysiol 75: 97-108, 1996.
43. Nusbaum MP, Marder AE. Modulatory proctolin-containing neuron (MPN). II. State-dependent modulation of rhythmic motor activity. J Neurosci 9: 1600-1607, 1989.
44. Nusbaum MP, Beenhakker MP. A small-systems approach to motor pattern generation. Nature 417: 343-350, 2002.
45. Rosen SC, Teyke T, Miller MW, Weiss KR, Kupfermann I. Identification and characterization of cerebral-to-buccal interneurons implicated in the control of motor programs associated with feeding in Aplysia. J Neurosci 11: 3630-3655, 1991.
46. Sakurai A, Katz PS. State-, timing-, and pattern-dependent neuromodulation of synaptic strength by a serotonergic interneuron. J Neurosci 29: 268-279, 2009.
47. Shaw AC, Jackson AW, Holmes T, Thurman S, Davis GR, McClellan AD. Descending brain neurons in larval lamprey: spinal projection patterns and initiation of locomotion. Exp Neurol 224: 527-541, 2010.
48. Smarandache CR, Daur N, Hedrich UB, Stein W. Regulation of motor pattern frequency by reversals in proprioceptive feedback. Eur J Neurosci 28: 460-474, 2008.
49. Soffe SR, Roberts A, Li WC. Defining the excitatory neurons that drive the locomotor rhythm in a simple vertebrate: insights into the origin of reticu- lospinal control. J Physiol 587: 4829-4844, 2009.
50. Stein W. Modulation of stomatogastric rhythms. J Comp Physiol A 195: 989-1009, 2009.
51. Stein W, Eberle CC, Hedrich UB. Motor pattern selection by nitric oxide in the stomatogastric nervous system of the crab. Eur J Neurosci 21: 2767- 2781,2005.
52. Stein W, Smarandache CR, Nickmann M, Hedrich UB. Functional conse- quences of activity-dependent synaptic enhancement at a crustacean neuro- muscular junction. J Exp Biol 209: 1285-1300, 2006.
53. Stein W, DeLong ND, Wood DE, Nusbaum MP. Divergent co-transmitter actions underlie motor pattern activation by a modulatory projection neuron. Eur J Neurosci 26: 1148-1165, 2007.
54. Takahashi M, Narushima M, Oda Y. In vivo imaging of functional inhibi- tory networks on the mauthner cell of larval zebrafish. J Neurosci 22: 3929-3938, 2002.
55. Teyke T, Weiss KR, Kupfermann I. Activity of identified cerebral neuron correlates with food-induced arousal in Aplysia. Neurosci Lett 133: 307- 310,1991.
56. Teyke T, Xin Y, Weiss KR, Kupfermann I. Ganglionic distribution of inputs, and outputs of C-PR, a neuron involved in the generation of a food-induced arousal state in Aplysia. Invert Neurosci 2: 235-244, 1997.
57. Weimann JM, Meyrand P, Marder E. Neurons that form multiple pattern generators: identification and multiple activity patterns of gastric/pyloric neurons in the crab stomatogastric system. J Neurophysiol 65: 111-122, 1991.
58. Wood DE, Manor Y, Nadim F, Nusbaum MP. Intercircuit control via rhythmic regulation of projection neuron activity. J Neurosci 24: 7455- 7463,2004.
59. Zelenin PV. Activity of individual reticulospinal neurons during different forms of locomotion in the lamprey. Eur J Neurosci 22: 2271-2282, 2005.
60. Zottoli SJ. Correlation of the startle reflex and Mauthner cell auditory responses in unrestrained goldfish. J Exp Biol 66: 243-254, 1997